Source identification of nitrous oxide emission pathways from a single-stage nitritation-anammox granular reactor

Water Research

Volumn 102, Issue , 2016, Pages 147-157

  Ali, Muhammad ^a,b   Rathnayake, Rathnayake M L D ^a,c   Zhang, Lei ^a   Ishii, Satoshi ^a,d   Kindaichi, Tomonori ^e   Satoh, Hisashi ^a   Toyoda, Sakae ^f   Yoshida, Naohiro ^f   Okabe, Satoshi ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

^b KING ABDULLAH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Saudi Arabia)

^c UNIVERSITY OF PERADENIYA   (Sri Lanka)

^d UNIVERSITY OF MINNESOTA   (United States)

^e HIROSHIMA UNIVERSITY   (Japan)

^f TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

Author keywords

FISH; Microsensors; N 2 O isotopomer analysis; N 2 O production pathway; Nitritation anammox reactor

Indexed keywords

ACTIVATED SLUDGE PROCESS; BATCH REACTORS; DENITRIFICATION; FISH; ISOMERS; ISOTOPES; MICROSENSORS; NITRIFICATION; NITROGEN OXIDES; WASTEWATER TREATMENT;

ANAMMOX REACTOR; BIOLOGICAL NITROGEN REMOVAL PROCESS; FLUORESCENT IN SITU HYBRIDIZATION; HETEROTROPHIC DENITRIFICATION; HETEROTROPHIC DENITRIFIERS; ISOTOPOMER ANALYSIS; PRODUCTION PATHWAYS; SEQUENCING BATCH REACTORS;

NITROGEN REMOVAL;

NITROUS OXIDE; RNA 16S; NITROGEN;

AMMONIUM; ANOXIC CONDITIONS; BIOMASS; BIOREACTOR; CYTOGENETICS; DENITRIFICATION; EMISSION CONTROL; GRANULAR MEDIUM; HETEROTROPHY; ISOTOPIC COMPOSITION; MICROBIAL COMMUNITY; NITROUS OXIDE; OXIC CONDITIONS; OXIDATION; POLLUTANT REMOVAL; SPATIAL DISTRIBUTION;

ANAMMOX BACTERIUM; ARTICLE; BIOMASS; BIOREACTOR; CARBON FOOTPRINT; CONCENTRATION AT STEADY-STATE; CONTROLLED STUDY; DENITRIFICATION; FLUORESCENCE IN SITU HYBRIDIZATION; ISOTOPE ANALYSIS; MICROBIAL ACTIVITY; MICROBIAL COMMUNITY; NEXT GENERATION SEQUENCING; NITRIFYING BACTERIUM; NITRITATION ANAMMOX GRANULAR REACTOR; NITROUS OXIDE EMISSION; NONHUMAN; OXIDATION; PRIORITY JOURNAL; REDUCTION; SEQUENCING BATCH REACTOR; WASTE COMPONENT REMOVAL; WASTE WATER MANAGEMENT; HETEROTROPHY; METABOLISM; OXIDATION REDUCTION REACTION;

BIOREACTORS; DENITRIFICATION; HETEROTROPHIC PROCESSES; NITROGEN; NITROUS OXIDE; OXIDATION-REDUCTION;

EID: 84975292935     PISSN: 00431354     EISSN: 18792448     Source Type: Journal    
DOI: 10.1016/j.watres.2016.06.034     Document Type: Article

References (69)

1. Ali M., Okabe S. Anammox-based technologies for nitrogen removal: advances in process start-up and remaining issues. Chemosphere 2015, 141:144-153.
2. Ali M., Oshiki M., Okabe S. Simple, rapid and effective preservation and reactivation of anaerobic ammonium oxidizing bacterium "Candidatus Brocadia sinica.". Water Res. 2014, 57:215-222.
3. Ali M., Oshiki M., Rathnayake L., Ishii S., Satoh H., Okabe S. Rapid and successful start-up of anammox process by immobilizing the minimal quantity of biomass in PVA-SA gel beads. Water Res. 2015, 79:147-157.
4. Caporaso J.G., Kuczynski J., Stombaugh J., Bittinger K., Bushman F.D., Costello E.K., Fierer N., Peña A.G., Goodrich J.K., Gordon J.I., Huttley G.A., Kelley S.T., Knights D., Koenig J.E., Ley R.E., Lozupone C.A., Mcdonald D., Muegge B.D., Pirrung M., Reeder J., Sevinsky J.R., Turnbaugh P.J., Walters W.A., Widmann J., Yatsunenko T., Zaneveld J., Knight R. Correspondence QIIME allows analysis of high- throughput community sequencing data Intensity normalization improves color calling in SOLiD sequencing. Nat. Publ. Gr 2010, 7:335-336.
5. Castro-Barros C.M., Daelman M.R., Mampaey K.E., van Loosdrecht M.C., Volcke E.I.P. Effect of aeration regime on N2O emission from partial nitritation-anammox in a full-scale granular sludge reactor. Water Res. 2015, 68:793-803.
6. Ciais P., Sabine C., Bala G., Bopp L., Brovkin V., Canadell J., Chhabra A., DeFries R., Galloway J., Heimann M., Jones C., Le Quéré C., Myneni R.B., Piao S., Thornton P. Carbon and other biogeochemical cycles. Climate Change 2013-The Physical Science Basis 2013, 465-570.
7. Colliver B.B., Stephenson T. Production of nitrogen oxide and dinitrogen oxide by autotrophic nitrifiers. Biotechnol. Adv. 2000, 18:219-232.
8. de Beer D., Stoodley P., Lewandowski Z. Measurement of local diffusion coefficients in biofilms by microinjection and confocal microscopy. Biotechnol. Bioeng. 1997, 53:151-158.
9. De Clippeleir H., Vlaeminck S.E., Mosquera M., Boeckx P., Verstraete W., Boon N. One-stage partial nitritation/anammox at 15 °C on pretreated sewage: feasibility demonstration at lab-scale. Appl. Microbiol. Biot. 2013, 97:10199-10210.
10. 2 O emissions. Water Res. 2011, 45:2811-2821.
11. 2 O emissions from biological nitrogen removal systems. Curr. Opin. Biotechnol. 2012, 23:474-482.
12. Domingo-Félez C., Mutlu A.G., Jensen M.M., Smets B.F. Aeration strategies to mitigate nitrous oxide emissions from single-stage nitritation/anammox reactors. Env. Sci. Technol. 2014, 48:8784-8792.
13. Elkins J.W. Determination of dissolved nitrous oxide in aquatic systems by gas chromatography using electtron-capture detection and multiple phase equilibration. Anal. Chem. 1980, 52:263-267.
14. Graaff M.S.De, Zeeman G., Temmink H., Loosdrecht M.C.M., Van de Graaff M.S., van Loosdrecht M.C.M., Buisman C.J.N. Long term partial nitritation of anaerobically treated black water and the emission of nitrous oxide. Water Res. 2010, 44:2171-2178.
15. Harris E., Joss A., Emmenegger L., Kipf M., Wolf B., Mohn J., Wunderlin P. Isotopic evidence for nitrous oxide production pathways in a partial nitritation-anammox reactor. Water Res. 2015, 83:258-270.
16. Herlemann D.P., Labrenz M., Jürgens K., Bertilsson S., Waniek J.J., Andersson A.F. Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISME J. 2011, 5:1571-1579.
17. Hu Z., Lotti T., De Kreuk M., Van Loosdrecht M., Kruit J., Mike S.M. Nitrogen removal by a nitritation-anammox bioreactor at low. Appl. Env. Microb. 2013, 79:2807-2812.
18. Ishii S., Song Y., Rathnayake L., Tumendelger A., Satoh H., Toyoda S., Yoshida N., Okabe S. Identification of key nitrous oxide production pathways in aerobic partial nitrifying granules. Env. Microbiol. 2014, 16:3168-3180.
19. Jinuntuya-Nortman M., Sutka R.L., Ostrom P.H., Gandhi H., Ostrom N.E. Isotopologue fractionation during microbial reduction of N2O within soil mesocosms as a function of water-filled pore space. Soil Biol. Biochem. 2008, 40:2273-2280.
20. Joss A., Salzgeber D., Eugster J., Roger K.O., Rottermann K., Burger S., Fabijan P., Leumann S., Mohn J., Siegrist H. Full-scale nitrogen removal from digester liquid with partial nitritation and anammox in one SBR. Env. Sci. Technol. 2009, 43:5301-5306.
21. Joss A., Derlon N., Cyprien C., Burger S., Szivak I., Traber J., Siegrist H., Morgenroth E. Combined nitritation-anammox: advances in understanding process stability. Environ. Sci. Technol. 2011, 45:9735-9742.
22. Kampschreur M.J., van der Star W.R.L., Wielders H.A., Mulder J.W., Jetten M.S.M., van Loosdrecht M.C.M. Dynamics of nitric oxide and nitrous oxide emission during full-scale reject water treatment. Water Res. 2008, 42:812-826.
23. Kampschreur M.J., Poldermans R., Kleerebezem R., van der Star W.R.L., Haarhuis R., Abma W.R., Jetten M.S.M., van Loosdrecht M.C.M., van der Star W.R.L., Haarhuis R., Abma W.R., Jetten M.S.M., van Loosdrecht M.C.M. Emission of nitrous oxide and nitric oxide from a full-scale single-stage nitritation-anammox reactor. Water Sci. Technol. 2009, 60:3211-3217.
24. Kampschreur M.J., Temmink H., Kleerebezem R., Jetten M.S.M., van Loosdrecht M.C.M. Nitrous oxide emission during wastewater treatment. Water Res. 2009, 43:4093-4103.
25. Kindaichi T., Yuri S., Ozaki N., Ohashi A. Ecophysiological role and function of uncultured Chloroflexi in an anammox reactor. Water Sci. Technol. 2012, 66:2556-2561.
26. Koba K., Fang Y., Mo J., Zhang W., Lu X., Liu L., Zhang T., Takebayashi Y., Toyoda S., Yoshida N., Suzuki K., Yoh M., Senoo K. The 15 N Natural Abundance of the N Lost from an N-saturated Subtropical Forest in Southern China 2012, 117:1-13.
27. Kong Q., Liang S., Zhang J., Xie H., Miao M., Tian L. N 2 O emission in a partial nitrification system: dynamic emission characteristics and the ammonium-oxidizing bacteria community. Bioresour. Technol. 2013, 127:400-406.
28. Kong Q., Zhang J., Miao M., Tian L., Guo N., Liang S. Partial nitrification and nitrous oxide emission in an intermittently aerated sequencing batch biofilm reactor. Chem. Eng. J. 2013, 217:435-441.
29. Kuenen J.G. Anammox bacteria: from discovery to application. Nat. Rev. Microbiol. 2008, 6:320-326.
30. Lackner S., Gilbert E.M., Vlaeminck S.E., Joss A., Horn H., van Loosdrecht M.C.M. Full-scale partial nitritation/anammox experiences-an application survey. Water Res. 2014, 55:292-303.
31. Law Y., Lant P., Yuan Z. The effect of pH on N 2 O production under aerobic conditions in a partial nitritation system. Water Res. 2011, 45:5934-5944.
32. Law Y., Ye L., Pan Y., Yuan Z. Nitrous oxide emissions from wastewater treatment processes. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 2012, 367:1265-1277.
33. Lorenzen J., Larsen L.H., Kjaer T., Revsbech N. Biosensor determination of the microscale distribution of nitrate, nitrate assimilation, nitrification, and denitrification in a diatom-inhabited freshwater sediment biosensor determination of the microscale distribution of nitrate, nitrate assimilati. Appl. Env. Microb. 1998, 64:3264-3269.
34. Lotti T., Kleerebezem R., Lubello C., van Loosdrecht M.C.M. Physiological and kinetic characterization of a suspended cell anammox culture. Water Res. 2014, 60:1-14.
35. Lu H., Chandran K. Factors promoting emissions of nitrous oxide and nitric oxide from denitrifying sequencing batch reactors operated with methanol and ethanol as electron donors. Biotechnol. Bioeng. 2010, 106:390-398.
36. Miura Y., Okabe S. Quantification of cell specific uptake activity of microbial products by uncultured chloroflexi by microautoradiography combined with fluorescence in situ hybridization. Environ. Sci. Technol. 2008, 42:7380-7386.
37. Miura Y., Watanabe Y., Okabe S. Significance of Chloroflexi in performance of submerged membrane bioreactors (MBR) treating municipal wastewater. Environ. Sci. Technol. 2007, 41:7787-7794.
38. Mulder A., Vandegraaf A.A., Robertson L.A., Kuenen J.G. Anaerobic ammonium oxidation discovered in a denitrifying fluidized-bed reactor. FEMS Microbiol. Ecol. 1995, 16:177-183.
39. Nielsen M., Bollmann A., Sliekers O., Jetten M., Schmid M., Strous M., Schmidt I., Larsen L.H., Nielsen L.P., Revsbech N.P. Kinetics, diffusional limitation and microscale distribution of chemistry and organisms in a CANON reactor. FEMS Microbiol. Ecol. 2005, 51:247-256.
40. Okabe S., Satoh H., Watanabe Y. In situ analysis of nitrifying biofilms as determined by in situ hybridization and the use of microelectrodes. Appl. Env. Microb. 1999, 65:3182-3191.
41. Okabe S., Oshiki M., Takahashi Y., Satoh H. N2O emission from a partial nitrification-anammox process and identification of a key biological process of N2O emission from anammox granules. Water Res. 2011, 45:6461-6470.
42. Okabe S., Oshiki M., Takahashi Y., Satoh H. Development of long-term stable partial nitrification and subsequent anammox process. Bioresour. Technol. 2011, 102:6801-6807.
43. Oshiki M., Shimokawa M., Fujii N., Satoh H., Okabe S. Physiological characteristics of the anaerobic ammonium-oxidizing bacterium "Candidatus Brocadia sinica.". Microbiology 2011, 157:1706-1713.
44. Oshiki M., Shinyako-Hata K., Satoh H., Okabe S. Draft genome sequence of an anaerobic ammonium-oxidizing Bacterium,"Candidatus brocadia sinica.". Genome Announc. 2015, 3:3-4.
45. Ostrom N.E., Piit A., Sutka R., Ostrom P.H., Grandy A.S., Huizinga K.M., Robertson G.P. Isotopologue effects during N2O reduction in soils and in pure cultures of denitrifiers. J. Geophys. Res. Biogeosciences 2007, 112:1-12.
46. Rathnayake R.M.L.D., Song Y., Tumendelger A., Oshiki M., Ishii S., Satoh H., Toyoda S., Yoshida N., Okabe S. Source identification of nitrous oxide on autotrophic partial nitrification in a granular sludge reactor. Water Res. 2013, 47:7078-7086.
47. Rathnayake R.M.L.D., Oshiki M., Ishii S., Segawa T., Satoh H., Okabe S. Effects of dissolved oxygen and pH on nitrous oxide production rates in autotrophic partial nitrification granules. Bioresour. Technol. 2015, 197:15-22.
48. Rodriguez-Caballero A., Pijuan M. N2O and NO emissions from a partial nitrification sequencing batch reactor: exploring dynamics, sources and minimization mechanisms. Water Res. 2013, 47:3131-3140.
49. Ross M.G., Russ C., Costello M., Hollinger A., Lennon N.J., Hegarty R., Nusbaum C., Jaffe D.B. Characterizing and measuring bias in sequence data. Genome Biol. 2013, 14:R51.
50. Satoh H., Miura Y., Tsushima I., Okabe S. Layered structure of bacterial and archaeal communities and their in situ activities in anaerobic granules. Appl. Environ. Microbiol. 2007, 73:7300-7307.
51. Schirrmeister B.E., Dalquen D.A., Anisimova M., Bagheri H.C. Gene copy number variation and its significance in cyanobacterial phylogeny. BMC Microbiol. 2012, 12:177.
52. Sliekers A.O., Derwort N., Gomez J.L.C., Strous M., Kuenen J.G., Jetten M.S.M. Completely autotrophic nitrogen removal over nitrite in one single reactor. Water Res. 2002, 36:2475-2482.
53. Strous M., Heijnen J.J., Kuenen J.G., Jetten M.S.M. The sequencing batch reactor as a powerful tool for the study of slowly growing anaerobic ammonium-oxidizing microorganisms. Appl. Microbiol. Biot. 1998, 50:589-596.
54. Sutka R.L., Ostrom N.E., Ostrom P.H., Breznak J.A., Pitt A.J., Li F., Gandhi H. Distinguishing nitrous oxide production from nitrification and denitrification on the basis of isotopomer abundances distinguishing nitrous oxide production from nitrification and denitrification on the basis of isotopomer abundances. Appl. Environ. Microbiol. 2006, 72:638-644.
55. Toyoda S., Yoshida N. Determination of Nitrogen Isotopomers of Nitrous 1999, 71:4711-4718.
56. Toyoda S., Mutobe H., Yamagishi H., Yoshida N., Tanji Y. Fractionation of N2O isotopomers during production by denitrifier. Soil Biol. Biochem. 2005, 37:1535-1545.
57. 4 in an advanced wastewater treatment system. Env. Sci. Technol. 2011, 45:917-922.
58. 2 O emitted from temperate agricultural soils determined via isotopomer ratio analysis. Glob. Biogeochem. Cycles 2011, 25:1-17.
59. Tsushima I., Kindaichi T., Okabe S. Quantification of anaerobic ammonium-oxidizing bacteria in enrichment cultures by real-time PCR. Water Res. 2007, 41:785-794.
60. van de Graaf A.A., Mulder A., De Bruijn P., Jetten M.S., Robertson L.A., Kuenen J.G. Anaerobic oxidation of ammonium is a biologically mediated process. These include: anaerobic oxidation of ammonium is a biologically mediated process. Appl. Env. Microb. 1995, 61:1246-1251.
61. Vázquez-Padín J., Fernádez I., Figueroa M., Mosquera-Corral A., Campos J.-L., Méndez R. Applications of Anammox based processes to treat anaerobic digester supernatant at room temperature. Bioresour. Technol. 2009, 100:2988-2994.
62. Vázquez-Padín J., Mosquera-Corral A., Campos J.L., Méndez R., Revsbech N.P. Microbial community distribution and activity dynamics of granular biomass in a CANON reactor. Water Res. 2010, 44:4359-4370.
63. Wrage N., Velthof G.L., Van Beusichem M.L., Oenema O. Role of nitrifier denitrification in the production of nitrous oxide. Soil Biol. Biochem. 2001, 33:1723-1732.
64. 2 O production in biological wastewater treatment under nitrifying and denitrifying conditions. Water Res. 2012, 46:1027-1037.
65. 2 O producing pathways in wastewater treatment. Environ. Sci. Technol. 2013, 47:1339-1348.
66. Wunderlin P., Siegrist H., Joss A. Online N2O measurement: the next standard for controlling biological ammonia oxidation?. Environ. Sci. Technol. 2013, 47:9567-9568.
67. Xiao P., Cai Q., Zhang D., Lu P. Characteristics of Nitrogen Removal and Nitrous Oxide Production in CANON Process 2013.
68. Yamagishi H., Westley M.B., Popp B.N., Toyoda S., Yoshida N., Watanabe S., Koba K., Yamanaka Y. Role of nitrification and denitrification on the nitrous oxide cycle in the eastern tropical North Pacific and Gulf of California. J. Geophys. Res. 2007, 112:1-15.
69. Yang J., Trela J., Plaza E., Tjus K. N 2 O emissions from a one stage partial nitri fi cation/anammox process in moving bed bio fi lm reactors. Water Sci. Technol. 2013, 68:144-152.